{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,7]],"date-time":"2025-11-07T13:35:43Z","timestamp":1762522543211,"version":"build-2065373602"},"reference-count":35,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2020,12,31]],"date-time":"2020-12-31T00:00:00Z","timestamp":1609372800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004271","name":"Sapienza Universit\u00e0 di Roma","doi-asserted-by":"publisher","award":["AR120172A8FD7E2B"],"award-info":[{"award-number":["AR120172A8FD7E2B"]}],"id":[{"id":"10.13039\/501100004271","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Life"],"abstract":"<jats:p>Whipworms are parasitic intestinal nematodes infecting mammals, and traditionally humans and other primates that have so far been considered infected by Trichuris trichiura. Recent molecular studies report a more complex scenario suggesting the presence of a species complex with several Trichuris taxa specifically infecting only one primate species as well as taxa able to infect a range of primate species. The systematics of the group is important for taxonomic inference, to estimate the relative zoonotic potential, and for conservation purposes. In fact, captive animals living in zoological gardens are usually infected by persistent monoxenous intestinal parasites. Here, two Japanese macaques living in the Bioparco Zoological Garden of Rome were found infected by Trichuris sp. Nematodes were characterized at the molecular level using nuclear (btub and 18S) and mitochondrial (16S and cytb) markers and then compared to Trichuris collected previously in the same location, and to other Trichuris infecting primates. Evidences from mitochondrial and nuclear markers allowed for the identification of Trichuris sp. specific to Macaca fuscata. Results obtained here also described a uniform taxonomic unit of Trichuris, separated but closely related to Trichuris trichiura, thus, emphasizing its zoonotic potential for workers and visitors.<\/jats:p>","DOI":"10.3390\/life11010018","type":"journal-article","created":{"date-parts":[[2020,12,31]],"date-time":"2020-12-31T10:10:37Z","timestamp":1609409437000},"page":"18","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Nuclear and Mitochondrial Data on Trichuris from Macaca fuscata Support Evidence of Host Specificity"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2245-9694","authenticated-orcid":false,"given":"Serena","family":"Cavallero","sequence":"first","affiliation":[{"name":"Department of Public Health and Infectious Diseases, Sapienza University of Rome, Piazzale Aldo Moro 5, 00185 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Margherita","family":"Montalbano Di Filippo","sequence":"additional","affiliation":[{"name":"Department of Clinical Sciences and Translational Medicine, University of Rome Tor Vergata, Via Montpellier 1, 00133 Rome, Italy"},{"name":"Istituto Superiore di Sanit\u00e0\u2014Viale Regina Elena 299, 00161 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0928-4110","authenticated-orcid":false,"given":"Silvia","family":"Rond\u00f3n","sequence":"additional","affiliation":[{"name":"Department of Public Health and Infectious Diseases, Sapienza University of Rome, Piazzale Aldo Moro 5, 00185 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Claudio De","family":"Liberato","sequence":"additional","affiliation":[{"name":"Istituto Zooprofilattico Sperimentale del Lazio e della Toscana \u201cM. Aleandri\u201d, Via Appia Nuova 1411, 00178 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1871-9553","authenticated-orcid":false,"given":"Stefano","family":"D\u2019Amelio","sequence":"additional","affiliation":[{"name":"Department of Public Health and Infectious Diseases, Sapienza University of Rome, Piazzale Aldo Moro 5, 00185 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Klaus G.","family":"Friedrich","sequence":"additional","affiliation":[{"name":"Fondazione Bioparco di Roma, Piazzale del Giardino Zoologico 1, 00197 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3952-4787","authenticated-orcid":false,"given":"Federica","family":"Berrilli","sequence":"additional","affiliation":[{"name":"Department of Clinical Sciences and Translational Medicine, University of Rome Tor Vergata, Via Montpellier 1, 00133 Rome, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2020,12,31]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1016\/j.vetpar.2007.06.020","article-title":"Gastrointestinal protozoa in non-human primates of four zoological gardens in Belgium","volume":"148","author":"Levecke","year":"2007","journal-title":"Vet. Parasitol."},{"key":"ref_2","unstructured":"Fowler, M., and Miller, R. (2014). New world and old world monkeys. Zoo and Wild Animal Medicine, Elsevier Saunders."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"83","DOI":"10.4038\/cjs.v45i1.7367","article-title":"Coprological survey of gastrointestinal parasites of mammals in Dehiwala National Zoological Gardens, Sri Lanka","volume":"45","author":"Aviruppola","year":"2016","journal-title":"Ceylon J. Sci."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"237","DOI":"10.2478\/s11686-019-00145-6","article-title":"Gastrointestinal parasites in captive animals at the Rio de Janeiro zoo","volume":"65","author":"Pinheiro","year":"2020","journal-title":"Acta Parasitol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1111\/jmp.12170","article-title":"Prevalence of gastrointestinal parasites in captive non-human primates of twenty-four zoological gardens in China","volume":"44","author":"Li","year":"2015","journal-title":"J. Med. Primatol."},{"key":"ref_6","unstructured":"Yamaguti, S. (1962). The nematodes of Vertebrates. Systema Helminthum, Interscience (Wiley)."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1521","DOI":"10.1016\/S0140-6736(06)68653-4","article-title":"Soil-Transmitted helminth infections: Ascariasis, trichuriasis, and hookworm","volume":"367","author":"Bethony","year":"2006","journal-title":"Lancet"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Ravasi, D.F., O\u2019Riain, M.J., Davids, F., and Illing, N. (2012). Phylogenetic evidence that two distinct Trichuris genotypes infect both humans and non-human primates. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0044187"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1007\/s00436-015-4748-9","article-title":"Study of the gastrointestinal parasitic fauna of captive non-human primates (Macaca fascicularis)","volume":"115","author":"Zanzani","year":"2016","journal-title":"Parasitol. Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1016\/j.meegid.2015.06.009","article-title":"Genetic heterogeneity and phylogeny of Trichuris spp. from captive non-human primates based on ribosomal DNA sequence data","volume":"34","author":"Cavallero","year":"2015","journal-title":"Infect. Genet. Evol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.vetpar.2019.06.019","article-title":"Insights into the molecular systematics of Trichuris infecting captive primates based on mitochondrial DNA analysis","volume":"272","author":"Cavallero","year":"2019","journal-title":"Vet. Parasitol."},{"key":"ref_12","first-page":"42","article-title":"Efficacy of fenbendazole and milbemycin oxime for treating baboons (Papio cynocephalus anubis) infected with Trichuris trichiura","volume":"46","author":"Reichard","year":"2007","journal-title":"J. Am. Assoc. Lab. Anim. Sci."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Montalbano Di Filippo, M., Berrilli, F., De Liberato, C., Di Giovanni, V., D\u2019Amelio, S., Friedrich, K.G., and Cavallero, S. (2020). Molecular characterization of Trichuris spp. from captive animals based on mitochondrial markers. Parasitol. Int., 75.","DOI":"10.1016\/j.parint.2019.102043"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1017\/S0031182000041202","article-title":"Morphological and histochemical study of Trichuris suis (Schrank, 1788) with special reference to the host-parasite relationship","volume":"61","author":"Jenkins","year":"1970","journal-title":"Parasitology"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1292\/jvms.55.363","article-title":"Comparative study of Trichuris trichiura from non-human primates and from man, and their difference with T. suis","volume":"55","author":"Ooi","year":"1993","journal-title":"J. Vet. Med. Sci."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Liu, G.H., Gasser, R.B., Su, A., Nejsum, P., Peng, L., Lin, R.Q., Li, M.W., Xu, M.J., and Zhu, X.Q. (2012). Clear genetic distinctiveness between human- and pig-derived Trichuris based on analyses of mitochondrial datasets. PLoS Negl. Trop. Dis., 6.","DOI":"10.1371\/journal.pntd.0001539"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.vetpar.2012.03.004","article-title":"Genetic analysis of Trichuris suis and Trichuris trichiura recovered from humans and pigs in a sympatric setting in Uganda","volume":"188","author":"Nissen","year":"2012","journal-title":"Vet. Parasitol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13071-015-0782-9","article-title":"Genetic analysis of Trichuris trichiura and Trichuris suis from Ecuador","volume":"8","author":"Meekums","year":"2015","journal-title":"Parasites Vectors"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Nei, M., and Kumar, S. (2000). Molecular Evolution and Phylogenetics, Oxford University Press.","DOI":"10.1093\/oso\/9780195135848.001.0001"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1870","DOI":"10.1093\/molbev\/msw054","article-title":"MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets","volume":"33","author":"Kumar","year":"2016","journal-title":"Mol. Biol. Evol."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Hawash, M., Betson, M., Al-Jubury, A., Ketzis, J., LeeWillingham, A., Bertelsen, M., Cooper, P., Littlewood, D., Zhu, X., and Nejsum, P. (2016). Whipworms in humans and pigs: Origins and demography. Parasites Vectors, 9.","DOI":"10.1186\/s13071-016-1325-8"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Liu, G., Gasser, R., Nejsum, P., Wang, Y., Chen, Q., Song, H., and Zhu, X. (2013). Mitochondrial and nuclear ribosomal DNA evidence supports the existence of a new Trichuris species in the endangered francois\u2019 leaf-monkey. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0066249"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Hawash, M.B.F., Andersen, L.O., Gasser, R.B., Stensvold, C.R., and Nejsum, P. (2015). Mitochondrial genome analyses suggest multiple Trichuris species in humans, baboons, and pigs from different geographical regions. PLoS Negl. Trop. Dis., 9.","DOI":"10.1371\/journal.pntd.0004059"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"4591","DOI":"10.1007\/s00436-015-4705-7","article-title":"Nuclear and mitochondrial genes for inferring Trichuris phylogeny","volume":"114","author":"Cutillas","year":"2015","journal-title":"Parasitol. Res."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Rivero, J., Garc\u00eda-S\u00e1nchez, \u00c1.M., Zurita, A., Cutillas, C., and Callej\u00f3n, R. (2020). Trichuris trichiura isolated from Macaca sylvanus: Morphological, biometrical, and molecular study. BMC Vet. Res., 16.","DOI":"10.1186\/s12917-020-02661-4"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1073","DOI":"10.1016\/j.ijpara.2014.08.010","article-title":"Mitochondrial genomes of Trichinella species and genotypes\u2014A basis for diagnosis, and systematic and epidemiological explorations","volume":"44","author":"Mohandas","year":"2014","journal-title":"Int. J. Parasitol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1093\/genetics\/157.2.621","article-title":"Trichinella spiralis mtDNA: A nematode mitochondrial genome that encodes a putative ATP8 and normally structured tRNAS and has a gene arrangement relatable to those of coelomate metazoans","volume":"157","author":"Lavrov","year":"2001","journal-title":"Genetics"},{"key":"ref_28","first-page":"111","article-title":"Beta-Tubulin gene from Trichuris trichiura","volume":"103","author":"Bennet","year":"1999","journal-title":"Mol. Biochem. Parasitol."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Hansen, T., Thamsborg, S., Olsen, A., and Nejsum, P. (2013). Genetic variations in the beta-tubulin gene and the internal transcribed spacer (ITS-2) region of Trichuris species from man and baboons. Parasites Vectors, 236.","DOI":"10.1186\/1756-3305-6-236"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1038\/ng.769","article-title":"The draft genome of the parasitic nematode Trichinella spiralis","volume":"43","author":"Mitreva","year":"2011","journal-title":"Nat. Genet."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"253","DOI":"10.3347\/kjp.2012.50.3.253","article-title":"Molecular identification of Oesophagostomum and Trichuris eggs isolated from wild Japanese macaques","volume":"50","author":"Arizono","year":"2012","journal-title":"Korean J. Parasitol."},{"key":"ref_32","unstructured":"Putaporntip, C., and Jongwutiwes, S. (2010). Detection of Trichuris trichiura and T. vulpis in human and dog stool samples by nested PCR. Asian Biomed., 4."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"39","DOI":"10.4269\/ajtmh.17-0651","article-title":"Molecular identification of Trichuris suis and Trichuris trichiura eggs in human populations from Thailand, Lao PDR, and Myanmar","volume":"98","author":"Phosuk","year":"2018","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_34","unstructured":"Li, D., Wang, X., and Song, M. (2020, December 30). Cloning and Sequence Analysis of the 18S Ribosomal RNA Gene from Five Isolates of Trichinella. Unpublished, Available online: https:\/\/www.ncbi.nlm.nih.gov\/nuccore\/AY497012."},{"key":"ref_35","first-page":"1","article-title":"How many species of whipworms do we share? Whipworms from man and other primates form two phylogenetic lineages","volume":"62","author":"Jirku","year":"2015","journal-title":"Folia Parasitol."}],"container-title":["Life"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-1729\/11\/1\/18\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:48:15Z","timestamp":1760179695000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-1729\/11\/1\/18"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,12,31]]},"references-count":35,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,1]]}},"alternative-id":["life11010018"],"URL":"https:\/\/doi.org\/10.3390\/life11010018","relation":{},"ISSN":["2075-1729"],"issn-type":[{"type":"electronic","value":"2075-1729"}],"subject":[],"published":{"date-parts":[[2020,12,31]]}}}